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Ecological Stoichiometry for Parasitologists

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Ecological Stoichiometry for Parasitologists Opinion Ecological Stoichiometry for Parasitologists 1, 2 Randall J. Bernot * and Robert Poulin Ecological stoichiometry (ES) is an ecological theory used to study the imbal- Highlights ances of chemical elements, ratios, and flux rates among organisms and the ES uses the balance of multiple ele- ments and energy in organisms and environment to better understand nutrient cycling, energy flow, and the role of their environment to understand nutri- organisms in ecosystems. Parasitologists can use this framework to study ent cycling and energy flow in ecolo- gical systems. phenomena across biological scales from genomes to ecosystems. By using the common currency of elemental ratios such as carbon:nitrogen:phosphorus, ES is a powerful framework for para- – parasitologists are beginning to explicitly link parasite host interactions to sitologists because it uses a common currency that cuts across biological ecosystem dynamics. Thus, ecological stoichiometry provides a framework scales from genes to ecosystems. for studying the feedbacks of parasites on the environment as well as the effects of the environment on parasites and disease. Parasitologists can use ES to answer questions ranging from topics that have already been well studied, but Why Ecological Stoichiometry? from new angles, to new frontiers in disease ecology and epidemiology. Ecological stoichiometry (ES) (see Glossary) is a framework for understanding ecological dynamics (i.e., the changing nature of ecological systems) by using first principles of chemistry and the balance among multiple elements and energy [1]. As a theory, ES has matured to help provide predictions about cellular, organismal, evolutionary, and ecosystem dynamics across a range of systems [2]. Parasitology is a field that can benefit from an ES approach by providing a basis for directly linking parasites to the broader ecological systems in which they are embedded, as well as understanding parasite–host interactions at multiple levels of organiza- tion. By framing parasite–host interactions in elemental ratios, as ES does, parasitologists can directly scale-up across biological levels by using the same metrics of nutrient cycling and energy flow as those used by ecosystem ecologists. Thus, key environmental drivers of parasitism and the potentially important feedbacks of parasites on ecosystems can be better understood using ES. In this Opinion article, we (i) give a brief primer on ES for parasitologists, (ii) present a conceptual framework of ES that illustrates the potential ways in which parasitologists can use ES, and (iii) outline ongoing and future questions that can be addressed with ES while reviewing a handful of recent examples from the literature. What Is Ecological Stoichiometry? Stoichiometry is the study of patterns of mass balance in the chemical conversions of different types of matter [3]. Many people are introduced to, and use, stoichiometry when balancing chemical reactions in introductory chemistry classes. These principles of mass balance are also widely used by ecologists to study nutrient cycling and energy flow in natural systems [1,3]. Carbon, nitrogen, and phosphorus are the elements most studied using the ES framework as they comprised the Redfield ratio [4], and C can be a useful proxy for energy while N and P are often 1 Department of Biology, Ball State limiting nutrients for organisms and ecosystems. Vannatta and Minchella [5] built a strong University, Muncie, IN 47306, USA 2 frameworkonwhichtounderstandparasite effectsonecosystemnutrient cycling.This framework Department of Zoology, University of Otago, Dunedin, New Zealand involves focusing on one nutrient at a time and can be a starting point for incorporating multiple nutrients and their ratios, as well as alterations in nutrient flux rates associated with altered host physiology and behavior. Additionally, other elements besides C, N, and P may be limiting in other *Correspondence: cases and thus worthy of explicit attention in an ES framework. For example, potassium has been [email protected] (R.J. Bernot). 928 Trends in Parasitology, November 2018, Vol. 34, No. 11 https://doi.org/10.1016/j.pt.2018.07.008 © 2018 Elsevier Ltd. All rights reserved. linked to fungal epidemics [6], and iron has long been studied for its role in infectious disease [7]. Glossary Theratios ofthese and other micronutrients may play a role in both host and parasite homeostasis. Connectance: in a food web, connectance is the proportion of realized feeding links out of all the Many organisms are adapted to maintain a homeostasis of elements needed for growth and possible feeding links. reproduction, deviations from which reduce fitness [8]. In other words, many animals need to obtain a Consumer-driven nutrient consistent ratio of essential nutrients from their food. When food nutrient ratios differ from the recycling (CNR): the feedback consumer’s homeostatic needs, a nutritional imbalance may result where one or more elemental mechanism linking consumer dynamics and producer nutritional nutrients limit growth or impair fitness. The animal then conserves the limiting nutrient while removing status. excess nonlimiting nutrients (Figure 1). Thus, animals often release or regenerate (through excretion or Ecological stoichiometry (ES): the egestion) nutrient elements at ratios different from those at which they ingest, leading to differential balance of multiple chemical elements during ecological nutrient availability in the environment [1]. These limitations can be predicted using the mass balance interactions. of the elements. Food chain length: the number of species encountered as energy or The relative amounts of essential elements or their ratio can determine nutrient use and cycling nutrients move from plants to top predators in a food web. The rates rather than their absolute amounts. In turn, differential nutrient regeneration at one trophic number of links between the base of level can affect other trophic levels and the broader ecosystem processes of nutrient cycling the web and the top predator. and energy flow [3]. Importantly, ES has provided insights into large-scale biogeochemical Growth rate hypothesis (GRH): couplings of organisms at the ecosystem scale [9] while also guiding questions at the genomic differences in organismal C:N:P ratios are caused by differential and cellular end of the biological scale (reviewed in [1]). For example, freshwater snails allocations to RNA necessary to exacerbated phosphorus limitation in a stream ecosystem through high N:P excretion ratios meet protein synthesis demands of (i.e., less P per unit N) of individual snails, thus linking individual elemental use and ecosystem rapid biomass growth and elemental cycling [10]. At the genomic scale, the elemental content of proteins is a function of development. Homeostasis: maintenance of the level of their encoding genes such that proteins associated with highly expressed genes in constant internal conditions in the plants are low in nitrogen compared to proteins encoded by low-expression genes [11]. face of externally imposed variation. Consumer-driven nutrient recycling (CNR) [12,13], threshold elemental ratios (TERs) Metabolic theory of ecology [14], and the growth rate hypothesis (GRH) [15] have all developed as key ecological (MTE): the fundamental biological rate that governs most patterns in concepts through ES [16]. More recently, efforts to understand the evolutionary dynamics ecology is organism metabolic rate. of stoichiometric traits have further expanded the scope of ES as a theory [2]. For example, This theory is based on relationships fi populations of rotifers fed P-de cient algal diets rapidly adapted to P-limiting conditions in among metabolic rate, body size, and temperature. which they had greater fitness compared to individuals from populations on P-rich diets [17]. Nestedness: in a food web, the Ecological stoichiometric approaches have been primarily developed in aquatic systems, while degree to which species with few the analogous framework of nutritional geometry (NG), which also centers on organismal links are a subset of the links of homeostasis and functionally relevant biochemical currencies, has matured from behavioral other species, rather than a different set of links. ecology and terrestrial insect ecology [16]. Additionally, the metabolic theory of ecology Nutritional geometry (NG): (MTE), which uses energy as a currency that scales across biological levels, has a number of framework of nutritional ecology common assumptions and goals as ES and NG [18–21]. Current efforts are underway to linking animal physiology, behavior, synthesize these frameworks to potentially arrive at a powerful perspective to link organisms and demography with macronutrients and micronutrients such as with their environment via the common currencies of materials and energy at many levels of carbohydrates, lipids, and proteins. biological organization [16]. These theories have not been developed using parasites, but we Redfield ratio: the atomic ratio of contend that using parasites and their hosts to test hypotheses within these frameworks will C, N, and P found in ocean plankton refine and inform general ecological theory and advance parasitology. Many opportunities exist (C:N:P = 117:14:1). Named after Alfred C. Redfield who first described to not only test hypotheses from these theories using parasite systems, but to also inform more the ratio. traditional epidemiological approaches to parasitology and disease ecology. Thus, we can look Threshold
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